Ecology, 92(2), 2011, pp. 325–332 Ó 2011 by the Ecological Society of America Macronutrient content of plant-based food affects growth of a carnivorous arthropod 1,4 2 3 1 SHAWN M. WILDER, DAVID A. HOLWAY, ANDREW V. SUAREZ, AND MICKY D. EUBANKS 1Department of Entomology, Texas A&M University, College Station, Texas 77843 USA 2Division of Biological Sciences, University of California at San Diego, La Jolla, California 92093 USA 3Department of Entomology and Department of Animal Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801 USA Abstract. Many arthropods engage in mutualisms in which they consume plant-based foods including nectar, extrafloral nectar, and honeydew. However, relatively little is known about the manner in which the specific macronutrients in these plant-based resources affect growth, especially for carnivorous arthropods. Using a combination of laboratory and field experiments, we tested (1) how plant-based foods, together with ad libitum insect prey, affect the growth of a carnivorous ant, Solenopsis invicta, and (2) which macronutrients in these resources (i.e., carbohydrates, amino acids, or both) contribute to higher colony growth. Access to honeydew increased the production of workers and brood in experimental colonies. This growth effect appeared to be due to carbohydrates alone as colonies provided with the carbohydrate component of artificial extrafloral nectar had greater worker and brood production compared to colonies deprived of carbohydrates. Surprisingly, amino acids only had a slight interactive effect on the proportion of a colony composed of brood and negatively affected worker survival. Diet choice in the laboratory and field matched performance in the laboratory with high recruitment to carbohydrate baits and only slight recruitment to amino acids. The strong, positive effects of carbohydrates on colony growth and the low cost of producing this macronutrient for plants and hemipterans may have aided the evolution of food-for-protection mutualisms and help explain why these interactions are so common in ants. In addition, greater access to plant-based resources in the introduced range of S. invicta may help to explain the high densities achieved by this species throughout the southeastern United States. Key words: ant–hemipteran–plant mutualism; aphid honeydew; food for protection; Gossypium hirsutum; mutualisms; nectar; nutritional ecology; plant-based resources; red imported fire ant; Solenopsis invicta; Texas, USA. INTRODUCTION interactions and, more generally, the conditions under Mutualisms are widespread among plants and animals which mutualisms are formed and maintained. and can affect population and community dynamics For some consumers, the motivation for consuming (Bronstein 1994, Wa¨ckers et al. 2005). Many mutualisms plant-based foods is clear. For example, in active animals involve the transfer of resources (e.g., plant-based such as hummingbirds and adult Lepidoptera, plant- resources such as nectar, extrafloral nectar, and honey- based foods provide a key source of carbohydrates to fuel dew) in exchange for services (e.g., pollination or the high metabolic costs of flight (Hainsworth and Wolf protection) (Bronstein 1998, Stadler and Dixon 2005, 1972, Josens and Farina 1997). However, the importance Wa¨ckers et al. 2005). Resources provided by plants or of plant-based foods for the diet of other animals is less hemipterans typically contain high concentrations of well understood. For example, the high carbohydrate and carbohydrates and low concentrations of amino acids low amino acid content of plant-based foods seems (e.g., an average of 310 g/L for carbohydrates and 3 g/L inconsistent with the high nitrogen requirements hypoth- for amino acids; Blu¨thgen et al. 2004). However, there esized for carnivorous arthropods (White 1978, Fagan et can be over 100-fold variation in the concentrations of al. 2002, Denno and Fagan 2003, Fagan and Denno carbohydrates (4–986 g/L) and amino acids (0.02–26.7 2004). Yet, carnivorous arthropods frequently engage in g/L) in plant-based resources (Blu¨thgen et al. 2004). A mutualisms with plants and Hemiptera that produce better understanding of how such variation affects the plant-based resources and consumption of these foods growth and survival of consumers will provide insight has positive effects on activity level, longevity, and growth into the costs and benefits of participating in mutualistic (Eubanks 2005, Stadler and Dixon 2005, Wa¨ckers et al. 2005, Helms and Vinson 2008). It is not known whether the effects of plant-based foods on the performance of Manuscript received 25 March 2010; revised 7 June 2010; accepted 12 July 2010. Corresponding Editor: R. A. Raguso. carnivorous arthropods are due to the carbohydrates, 4 E-mail: [email protected] amino acids, or both. Experimental tests of how the 325 326 SHAWN M. WILDER ET AL. Ecology, Vol. 92, No. 2 macronutrient content of plant-based resources affects 2009. After 48 hours, water was used to separate carnivore performance may reveal whether the low amino workers, brood, and queens from the soil. This material acid content provides more of a benefit than would be was used to make standardized laboratory colonies that expected based on its concentration or whether carbohy- each consisted of 1–20 queens (to test the effects of drates are an underappreciated macronutrient for growth aphid honeydew on colony growth) or two queens (to of carnivorous arthropods. In addition, the effects of test the effects of carbohydrates and amino acids on carbohydrates and amino acids on carnivore performance growth), ;50 brood and 1 g wet mass of workers (0.345 may provide insight into the likelihood with which 6 0.009 g dry mass or 1192 6 62 individuals; mean 6 1 individuals should engage in mutualisms with plants or SE). Polygyne colonies in the field vary in the number of hemipterans that provide different concentrations of queens present (Tschinkel 2006). However, the number these macronutrients. of queens had no effect on colony size in experiment 1 Consumption of plant-based foods may also be (general linear model ANOVA, number of workers, important for the establishment and spread of invasive F1,28 ¼ 0.26, P ¼ 0.61; number of brood, F1,28 ¼ 0.45, P ¼ arthropods. Some invasive ants may have greater access 0.51). For this reason, we used two queens in each to plant-based resources in their introduced range than colony for experiment 2. Each colony from the field was in their native range (Tillberg et al. 2007). In the used to make a single laboratory replicate. Laboratory southeastern United States, the red imported fire ant colonies were housed in containers (56 cm length 3 40 (Solenopsis invicta) is responsible for significant ecolog- cm width 3 14 cm height) lined with fluon and provided ical, health, and economic impacts (Tschinkel 2006). with a darkened petri dish lined with plaster of paris for Solenopsis invicta is a carnivorous ant that primarily a nest. Colonies were provided with a vial of water and consumes animal tissue and haemolymph and has a had the plaster of paris substrate moistened two times 15 d N stable isotope signature similar to that of obligate per week. Each colony was provided with two freshly predators, such as spiders (Tennant and Porter 1991, killed crickets, Acheta domesticus, three times per week, Vogt et al. 2002, Tillberg et al. 2007). However, S. which was ad libitum prey for colonies used in these invicta also frequently forms mutualisms with honey- experiments. The use of ad libitum insect prey is dew-producing hemipterans in their introduced range consistent with conditions in nature as colonies of S. (Helms and Vinson 2002) and these interactions invicta regularly dry and store pieces of insects in colony influence how S. invicta affects arthropod food webs chambers in the field (Gayahan and Tschinkel 2008). (Kaplan and Eubanks 2005). In addition, consumption The colony room was maintained on a 12:12 light : dark of honeydew increases colony growth rate of S. invicta, photoperiod with 40–70% humidity and a daily temper- although the mechanisms responsible for this increase ature cycle that included 8 h during daylight at 328C and (e.g., greater worker longevity, higher rates of brood 16 h at 248C. Colonies were maintained in the laboratory production, or both) remain unclear (Helms and Vinson for 45 d in experiment 1 and 60 d in experiment 2 after 2008). Testing how the macronutrient content of plant- which they were frozen. We then separated workers and based resources affects carnivorous arthropods may brood, dried them at 608C for 48 h, and weighed them. provide a better understanding of the spread, ecological impacts, and control of invasive species such as S. Effects of aphid honeydew on colony growth invicta. This laboratory experiment quantified the growth of The purpose of this study was to examine the benefits colonies of S. invicta in the presence of high and low of consuming plant-based resources for a carnivorous densities of aphids. Each container with fire ants insect, the red imported fire ant (Solenopsis invicta), and received three cotton plants, Gossypium hirsutum,in to test which nutritional components of plant-based 8.75 cm square plastic pots containing potting soil, in resources (i.e., carbohydrates, amino acids, or both) which S. invicta readily nested. The aphid treatment (n ¼ contributed to higher colony growth. In the first part of 15) was created by adding cotton aphids, Aphis gossypii, this study, we quantified the effects of aphid honeydew to plants and allowing populations to become estab- on worker and brood production of S. invicta colonies lished while the control treatment (n ¼ 17) was reared in the laboratory. In the second part of this study, maintained by searching cotton plants twice each week we separated the carbohydrate and amino acid compo- and killing any aphids found. Cotton plants had nents of artificial extrafloral nectar to test: (1) which extrafloral nectaries.